Skip to main content
Log in

A dioxygenase gene (Ids2) expressed under iron deficiency conditions in the roots of Hordeum vulgare

  • Research Article
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

A λzapII cDNA library was constructed from mRNA isolated from Fe-deficient barley roots and screened with cDNA probes made from mRNA of Fe-deficient and Fe-sufficient (control) barley roots. Seven clones were selected. Among them a clone having the putative full-length mRNA of dioxygenase as judged by northern hybridization was selected and named Ids2 (iron deficiency-specific clone 2). Using a cDNA fragment as probe, two clones from the genomic library (λEMBL-III) were isolated and one was sequenced. The predicted amino acid sequence of Ids2 resembled that of 2-oxoglutarate-dependent dioxygenase. Ids2 is expressed in the Fe-deficient barley roots but is not in the leaves. The expression is repressed by the availability of Fe. Ids2 was also strongly expressed under Mn deficiency and weakly under Zn deficiency or excess NaCl (0.5%). The upstream 5′-flanking region of Ids2 has a root-specific cis element of the CaMV 35S promoter and a nodule-specific element of leghemoglobin, a metal regulatory element (MRE) and several Cu regulatory elements (UAS) of yeast metallothionein (CUP1).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Butt TR, Sternberg EJ, Gorman JA, Clark P, Hamer D, Rosenberg M, Crooke ST: Copper metallothionein of yeast, structure of the gene and regulation of expression. Proc Natl Acad Sci USA 81: 3332–3336 (1984).

    Google Scholar 

  2. Bogusz D, Llewellyn DJ, Craig S, Dennis ES, Appleby CA, Peacock WJ: Nonlegume hemoglobin genes retain organ-specific expression in heterologous transgenic plants. Plant Cell 2: 633–641 (1990).

    Google Scholar 

  3. de Framond AJ: A metallothionein-like gene from maize (Zea mays), cloning and characterization. FEBS Lett 290: 103–106 (1991).

    Google Scholar 

  4. de Miranda JR, Thomas MA, Thruman DA, Tomsett AB: Metallothionein genes from the flowering plant Mimulus guttatus. FEBS Lett 260: 277–280 (1990).

    Google Scholar 

  5. Diekman J, Fischer RL: Interaction of a DNA binding factor with the 5′-flanking region of an ethyleneresponsive fruit ripening gene from tomato. EMBO J 7: 3315–3320 (1988).

    Google Scholar 

  6. Evans IM, Gatehouse LN, Gatehouse JA, Robinson NJ, Croy RRD: A gene from pea (Pisum sativum L.) with homology to metallothionein genes. FEBS Lett 262: 29–32 (1990).

    Google Scholar 

  7. Gasser CS, Budelier KA, Smith AG, Shah DM, Fraley RT: Isolation of tissue specific cDNAs from tomato pistils. Plant Cell 1: 15–24 (1989).

    Google Scholar 

  8. Hamilton AJ, Bouzayen M, Grierson D: Identification of a tomato gene for the ethylene-forming enzyme by expression in yeast. Proc Natl Acad Sci USA 88: 7434–7437 (1991).

    Google Scholar 

  9. Hashimoto T, Hayashi A, Amano Y, Kohno J, Iwanari H, Usuda S, Yamada Y: Hyoscyamine 6β-hydroxylase, an enzyme involved in tropane alkaloid biosynthesis, is localized at the pericycle of the roots. J Biol Chem 266: 4648–4653 (1991).

    Google Scholar 

  10. Holdsworth MJ, Bird CR, Ray J, Schuch W, Grierson D: Structure and expression of an ethylene related mRNA from tomato. Nucl Acids Res 15: 731–739 (1987).

    Google Scholar 

  11. Holdsworth MJ, Schuch W, Grierson D: Nucleotide sequence of an ethylene-related gene from tomato. Nucl Acids Res 15: 10600 (1987).

    Google Scholar 

  12. Imbert J, Culotta V, Furst P, Gedamu L, Hamer D: Regulation of metallothionein gene transcription by metals. In: Eichhorn GL, Marzilli LG (eds) Metal-ion Induced Regulation of Gene Expression vol. 8, pp. 159–164. Elsevier, Amsterdam (1990).

    Google Scholar 

  13. Irifune T, Hirano H, Umehara Y, Nishizawa N, Mori S: Partial amino acid sequence of a protein that appears in Fe-deficient barley roots. Abstracts of the 37th Meeting of Soil Science and Plant Nutrition (Japan) Part II, p. 272 (1991).

  14. Ishizuka K, Tanaka A, Fujita O: Studies on the nutrients metabolism in rice. 6. Effect of the concentration of Fe, Mn and Cu on the growth and the nutrients content of rice. J Soil Sci Plant Nutr 32: 97–100 (1961). (In Japanese.)

    Google Scholar 

  15. Kawashima I, Inokuchi Y, Chino M, Kimura M, Shimizu N: Isolation of a gene for a metallothionein-like protein from soybean. Plant Cell Physiol 32: 913–916 (1991).

    Google Scholar 

  16. Klausner FD, Rouault TA, Harfold JB: Regulating the fate of mRNA: the control of cellular iron metabolism. Cell 72: 19–28 (1993).

    Google Scholar 

  17. Kovacevic S, Weigel BJ, Tobin MB, Ingolia TD, Miller JR: Cloning, characterization and expression in Escherichia coli of the Streptomyces clevuligerus gene encoding deacetoxycephalosporin C synthetase. J Bact 171: 754–760 (1989).

    Google Scholar 

  18. Lam E, Benfey PN, Gilmartin PM, Fang R-X, Chua N-H: Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci USA 86: 7890–7894 (1989).

    Google Scholar 

  19. Lescure AM, Proudhon D, Pesey H, Ragland M, Theil EC, Briat JF: Ferritin gene transcription is regulated by iron in soybean cell cultures. Proc Natl Acad Sci USA 88: 8222–8226 (1991).

    Google Scholar 

  20. Lobreaux S, Massenet O, Briat JF: Iron induces ferritin synthesis in maize plantlets. Plant Mol Biol 19: 563–575 (1992).

    Google Scholar 

  21. Logmann J, Schell J, Willmitzer L: Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16–20 (1987).

    Google Scholar 

  22. Ma JF, Nomoto K: Two related biosynthetic pathways of mugineic acids in gramineous plants. Plant Physiol 102: 373–378 (1993).

    Google Scholar 

  23. Matsuda J, Okada S, Hashimoto T, Yamada Y: Molecular cloning of hytoscyamine 6β-hydroxylase, a 2-oxoglutarate-dependent dioxygenase, from cultured roots of Hyoscyamus niger. J Biol Chem 266: 9460–9464 (1991).

    Google Scholar 

  24. Menssen A, Hohmann S, Martin W, Schnable PS, Peterson PA, Saedler H, Gierl A: The En/Spm transposable element of Zea mays contains splice sites at the temini generating a novel intron from a dSpm element in the A2 gene. EMBO J 9: 3051–3057 (1990).

    Google Scholar 

  25. Mihashi S, Mori S: Characterization of mugineic acid-Fe transporter in Fe-deficient barley roots using the multicompartment transporter box method. Biol Meth 2: 146–154 (1989).

    Google Scholar 

  26. Mori S, Nishizawa N: Methionine as a dominant precursor of phytosiderophores in Graminaceae plants. Plant Cell Physiol 28: 1081–1092 (1987).

    Google Scholar 

  27. Mori S, Hachisuka M, Kawai S, Takagi S, Nishizawa NK: Peptides related to phytosiderophores secretion by Fe-deficient barley roots. J Plant Nutr 11: 653–662 (1988).

    Google Scholar 

  28. Mori S, Nishizawa N: Identification of barley chromosome No. 4, possible encoder of genes of mugineic acid synthesis from 2′-deoxymugineic acid using wheat barley addition lines. Plant Cell Physiol 30: 1057–1061 (1989).

    Google Scholar 

  29. Mori S, Nishizawa N, Fujigaki J: Identification of rye chromosome 5R as a carrier of the genes for mugineic acid synthetase and 3-hydroxymugineic acid synthetase using wheat-rye addition lines. Jpn J Genet 65: 343–352 (1990).

    Google Scholar 

  30. Nakanishi N, Okumura N, Umehara Y, Nishizawa NH, Chino M, Mori S: Expression of a gene specific for iron deficiency (Ids3) in the roots of Hordeum vulgare. Plant Cell Physiol 34: 401–410 (1993).

    Google Scholar 

  31. Neilands JB: Molecular aspects of regulation of high affinity iron absorption in microorganisms. In: Eichhom GL, Marzilli LG (eds) Metal-ion Induced Regulation of Gene Expression vol. 8, pp. 63–83. Elsevier, Amsterdam (1990).

    Google Scholar 

  32. Okumura N, Nishizawa NK, Umehara Y, Mori S: iron deficiency-specific cDNA from barley roots having two homologous cysteine-rich MT domains. Plant Mol Biol 17: 531–533 (1991).

    Google Scholar 

  33. Okumura N, Nishizawa NK, Umehara Y, Ohata T, Mori S: Iron deficiency specific cDNA (Ids1) with two homologous cysteine rich MT domains from the roots of barley. J Plant Nutr 15: 2157–2172 (1992).

    Google Scholar 

  34. Robinson NJ, Evans IM, Mulcrone J, Bryden J, Tommey AM: Genes with similarity to metallothionein genes and copper, zinc ligands in Pisum sativum L. Plant Soil 146: 291–298 (1992).

    Google Scholar 

  35. Römheld V, Marschner H: Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80: 175–180 (1986).

    Google Scholar 

  36. Rouault T, Tang CK, Kaptain S, Burgess WH, Haile DJ, Samaniego F, McBride OW, Harford JB, Klusner RD: Cloning of the cDNA encoding an RNA regulatory protein: the human iron-responsive element-binding protein. Proc Natl Acad Sci USA 87: 7958–7962 (1990).

    Google Scholar 

  37. Samson SM, Belagaje R, Blankenship DT, Chapman JL, Perry D, Sktrud PL, van Frank RM, Abraham EP, Baldwin JF, Queener Sw, Ingolia TD: Isolation, sequence determination and expression in Escherichia coli of the isopenicillin N synthetase gene from Cephalosporium acremonium. Nature 318: 191–194 (1985).

    Google Scholar 

  38. Samson SM, Datzlaf JE, Slisz ML, Becker GW, van Frank RM, Veal LE, Yeh W-K, Miller JR, Queener SW, Ingolia TD: Cloning and expression of the fungal expandase/hydroxylase gene involved in cephalosporin biosynthesis. Bio/technology 5: 1207–1213 (1987).

    Google Scholar 

  39. Sandal NN, Bojsen K, Marker KA: A small family of nodule-specific genes from soybean. Nucl Acids Res 15: 1507–1519 (1987).

    Google Scholar 

  40. Shojima S, Nishizawa NK, Fushiya S, Nozoe S, Irifune T, Mori S: Biosynthesis of Phytosiderophores. In vitro biosynthesis of 2′-deoxymugineic acid from L-methionine and nicotianamine. Plant Physiol 93: 1497–1503 (1990).

    Google Scholar 

  41. Smith VA, MacMillan J: The partial purification and characterization of gibberellin 2β-hydroxylases from seeds of Pisum sativum. Planta 167: 9–18 (1986).

    Google Scholar 

  42. Takagi S: Naturally occurring iron-chelating compounds in oat- and rice-root washing. I. Activity measurement and preliminary characterization. Soil Sci Plant Nutr 22: 423–433 (1976).

    Google Scholar 

  43. Takahashi K, Kawashima I, Chino M: Cloning of MT-like gene in Arabidopsis. Proceedings of the Annual Meeting and 31st Symposium, Japanese Society of Plant Physiologists, Okayama, p. 236 (1991).

    Google Scholar 

  44. Thiele D, Hamer KD: Tandemly duplicated upstream control sequences mediate copper-induced transcription of the Sacharomyces cerevisiae copper-metallothionein gene. Mol Cell Biol 6: 1158–1163 (1986).

    Google Scholar 

  45. Treeby M, Marschner H, Römheld V: Mobilization of iron and other micronutrient cations from a calcareous soil by plant-borne, microbial, and synthetic metal chelators. Plant Soil 114: 217–226 (1989).

    Google Scholar 

  46. Zang F, Römheld V, Marschner H: Role of the root apoplasm for iron acquisition by wheat plants. Plant Physiol 97: 1302–1305 (1991).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Okumura, N., Nishizawa, NK., Umehara, Y. et al. A dioxygenase gene (Ids2) expressed under iron deficiency conditions in the roots of Hordeum vulgare . Plant Mol Biol 25, 705–719 (1994). https://doi.org/10.1007/BF00029608

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00029608

Key words

Navigation